Exposure to a conditioned aversive environment interferes with long-term potentiation induction in the fimbria–CA3 pathway

Abstract

The effect of re-exposure of rats to an aversive environment on the induction of long-term potentiation was investigated in the CA3 region 3 and 12 h after contextual conditioning. Electrophysiological recordings showed that re-exposure of rats to the conditioning chamber produced a significant and long-lasting decrease in population spike amplitude at both post-conditioning delays. High-frequency stimulation of the fimbria induced a large and persistent increase in CA3 population spike amplitude (about 400% of baseline) in animals of control groups and shocked animals that were not re-exposed to the conditioning environment. However, high-frequency stimulation applied during re-exposure of shocked subjects 3 h after the initial exposure resulted in a small and transient increase in population spike amplitude (about 140% of baseline); when applied 12 h after the initial exposure, it produced a persistent depression of the response (−30% of baseline). Behavioural testing indicated that re-exposure of shocked animals to the conditioning environment elicited a qualitatively and quantitatively similar freezing behaviour at both post-conditioning delays (3 or 12 h). In contrast to the long-lasting decrease in CA3 population spike amplitude produced by re-exposure to the aversive environment, the level of freezing behaviour diminished rapidly within 10 min of exposure. These results suggest that, during exposure to a conditioned aversive environment, alterations in fimbria–CA3 neural processing may be dissociated from contextual fear-induced freezing behaviour. In addition, processes underlying long-term potentiation induction in fimbria–CA3 pathway may be opposite to those taking place during hippocampal processing of conditioned aversive contexts.